tivariate Analysis of Correlations Between Environmenta

Parameters and Cadmium Concentrations in Hyalella azteca

(Crustacea: Amphipoda) from Centra Ontario Lakes
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M. Stephenson1and C. L. Mackie
Department of Zoology, University of Cuelph, Guelph, Ont. N 9 C 2W1

Stephenson, M., and 6 . L. Mackie. 1988. Multivariate analysis of correlations between environmental parameters
and cadmium concentrations in Hyalella azteca (Crustacea: Amphipda) from central Ontario Bakes.
Can. j. Fish. Aquat. Sci. 45: 1705-1 75 0.
Cadmium concentrations in Hyalelda azteca collected from 69 central Ontario Bakes ranged from 8.1 3 to 56.6
kg/$dry mass. Principal components analysis followed by multiple linear regression found three principal components, interpreted as water hardness, total cadmium, and dissolved organic carbon concentrations, to be significantly (p =S 0.002) correlated with cadmium concentrations in H . azteca. Cadmium concentrations in H.
azteca were independent of cadmium concentrations in littoral sediments. It i s suggested that cadmium ions
compete with calcium ions for uptake sites on the gill surfaces of H. azteca. High concentrations of dissolved
organic carbon may complex free cadmium ions and reduce their concentration in solution, leading to lower
cadmium concentrations in H. azteca.
Les teneldrs en cadmium chez des specimens d'Hyalella azteca prelev6s dans 69 Bacs du centre de ItOntario
6taient comprises entre 0,13 et 56,6
de masse sGche. L'analyse des cornposantes principales suivie d'une
regression lineaire multiple a permis de dkceler une correlation significative (p
0,002) entre trois grandes
composantes (durete de I'eau, cadmium total et concentration en carbone organique dissous) et les teneurs en
cadmium relevees chez H. azteca. Les teneurs en cadmium chez H. azteca 6taient independantes de la teneur
en cadmium des sgdiments Iittoraux. Ces donnees semblent indiquer que les ions cadmium rivalisent avec les
ions calcium pour les sites de fixation la surface des branchies chez H. azteca. Des teneurs elevees en carbone
organique dissous peuvent former des complexes avec des ions cadmium libres et r a u i r e Jeur concentration
dans la solution, ce qui entraine des tenem en cadmium plus faibles chez 68. azteca.
R e p le 3 judlet 3987
Accept4 le 3 1 mai 3 988

Received july 3, 1987

Accepted May 3 7 , 1988

(J9.344)

xcept for a local area of high Cd deposition mew SSaabury,

h e central Ontaris region has a generally low and uniform
Cd deposition rate (Chan et al. 1986). However, low pH
has been shown to elevate Cd concentrations in Scandinavian
( H e d s e n and Wright 1978; Borg 1983) and Ontaris (Stephenson and Mackie 1988) lakes. Consquently, Cd concentrations in central Ontario sudace waters range from iaradetectable (<5 ng/E) to concentrations in excess of 588 ng/E
(Stephenson and Mackie 1988).
W i l e high envkonmentd Cd concentrations, chiefly in the
context of direct industrial contamination, have k e n related to
high concentrations of Cd in biota (Anderson et al. 1978; Kneip
and H a e n 1979; Zauke 1981, 1982a, 1982b; Jop and Wojtan
B982), few studies have examined factors modifying the availability sf Cd to biota in ecosystems remote from point sources
of contamhation.
This study examines the effects sf the chemical md morphornetfic characteristics of 69 central Ontario Precambrian
Shield lakes on Cd concentrations in the benthic amphipod
'Resent ad&ess: Department of Fisheries md Oceans, Freshwater
Institute, 501 University Crescent, Winnipeg, Man. W3T 2N6.
Can. J. Fish. Aquat. Sci., Vo1. 45, 1 9 8

Hyalella azteca. Correlations between Cd concentrations in

H. azteca and environmental parmeters were evaluated by
multiple linear regression after the environmental data were
reduced to orthogonal variables by principal components
analysis (PCB).

Methods
Seventy-five central Ontario lakes (Fig. 1) were sampled
between July 17, 1984, and August 15, 1984, by scraping surface sediments with a stainless-steel sieve (0.32 mm)md examining the sediments ret.eved for H. azteca. Hyalehla azteca!
was found in 69 lakes. Animals were sorted with stainless-steel
forceps into acid-cleaned polypropylene cups filled with clean
lake water. They were kept cool for 24 h to allow gut clearance
and then frozen in distilled-deionized water in acid-cleaned
polypropylene vials. The animals were subsequently thawed,
placed in acid-rinsed polystyrene tissue culture dishes (35 X
10 m),and examined under a dissecting microscope. Undmaged animals with 890 observable gut contents (10 per lake when
possible) were individually placed in acid-cleaned 1.5-mE
poiypropylene microcentrifuge tubes and oven dried (55C)

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FIG. 1 . Central Ontario showing the locations of the study lakes. The square in the inset map sf Canada
shows the approximate location of the study m a .

overnight. Empty vials to be used for analytical reagent blanks

were dried simultaneously. After drying, the mimds were individudly weighed ( & 5 pg) on a C& m d e l G2 eIectrobalmce.
Animals were wet-ashed in microcentrifuge tubes by adding
25 pH, of reagent-grade (70%) HNO,, followed after 1 wk by
18 pL of 50% H202.The digestate was subsequently diluted
with 1.0 IL of distilled-deionized water, giving a sample
matrix of 1 -7% HNO,. Reagent blanks and reference materials
were digested simultaneously. Digestate solutions were malysed by tungsten furnace atomic absorption spectrophotometry
(Scintrex AAZ-2 with 'Zeemm background correction). The
technique was tested by digesting and analyzing Cd concentrations in an NBS standard reference mderkd (1566 oyster tissue). Measured Cd concentrations (3.66 9 0.42 QSD) pg/g dry
mass) agreed with the certified value (3.5 pg/g dry mass.
Water samples were collected for routine chemical analysis
(Ca2+,Mg2+,Na+ , K + , Cl - , SO,'-, total Fe, total Mn, total
P,dissolved organic carbon (DOC)) by the Ontario Ministry of
the Environment, using techniques described in Ontario Ministry of the Environment (198 1). Lake vaea, perimeter, m d mean
and maximum depth were obtained (where possible) from the
Ontario Ministry of Natural Resources (Fisheries Branch, Environmentd a%ynmicsSection),
The data were reduced by PCA. The raw data (with the
exception of pH) were nnn-normal, so Iogarithmic trmsformations were applied. Box plots (Tukey 1977) indicated that
the transformed data were approximately normally distributed.
PCA's based upon the correlation matrices, and using vxirnax
rotations, were p r f o m e d on the nomdized data. Stepwise
(p 90.05) multiple linear regression was used with mean Cd
concentrations in H . azteca for each I&e as the dependent variable, and PCB scores fm each lake on each principal wmponent as independent variables, to identify environmental vvaiables correlated with Cd concentrations in H. azfeca.
1%M

Variables were removed from the data matrix if (1) they

loaded most strongly onto a rotated principal component which
was subsequently shown by linear regression to be mcomelated
ggP > 0005)with cadmium concentratisns in H . azteca m d ( 2 )
the mean-square error of the multiple regression run with principal components derived from the reduced data matrix was not
significantly different from the mem-squm error derived from
the original data matrix. The latter was tested using the F-amam
statistic (David 1952). In this way the original data matrix of
20 variables was reduced to 6 variables loading ow thee orthogonal principal components, each of which was significantly
('p d 0.002) correlated with Cd concentrations in H.azteea.

Cadmium concentrations in H. azteea from central Ontario

lakes ranged from 0.13 to 56.6 pg/g (Table 1). Water m d sediment c h e ~ s t r yand lake morphometric data were available for
51 lakes in which H. azteea was found. The 28 variables originally included in the PCA matrix and their means md ranges
are given in Table 2. These variables were reduced to six (Ca2+,
acid-neutralizing capacity (ANC), pH, Mg2+, DOC, total Cd),
loading on thee principal components, without any significant
(HP < 0.05) increase in the mean-square e m r of the regression
analysis of variance. The loadings of variables on the t h e e prim
cipd components are given in Table 3. These thee principal
components account for 94% of the overall variance of the sixvariable data set and a e interpreted as follows: PC1 = Water
hardness (Ca2+,Mg2+,ANC, pH); P I 2 = DOC; PC3 = total
Cd in water. The regression of Cd in H . azteea versus the K A
scores for each lake on each principal component is s u m a rized in Table 4. Each principal component is significantly correlated with Cd concentrations in H. wzteca, and none of the
retained variables can be rejected.
Can. S. fish. Aqua. Sci., Vsl. 45, 8988

TABLE1. Cd concentrations in Pi. aztem collected from lakes in centrd

Ontario. Unless otherwise noted in parentheses, the number given is
the mean of 18 detemimtions. NP indicates that H. azteca was not
found at the time of sampling.
Cd in Pi. azteca

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Lake
Richard
McFarlane
Raft
hhi
Clearwater
Simn
McCharles
Attlee
Gainey
Broker
Tyson
Mahzenazing
Kakakiwaganda

Township

H m

Dill
BroderIDill
DillIBroder
Broder
Broder
Graham
Grahm
Attlee
Attlw
Attlee
SalelAttlee
Humboldt
Servos
Bigwssd

Sollmm
Cecebe
Ahmic
Old Man's
Bell's (Silver)
Spence
Horn
Bear
Rdney
Bray
King
Eagle
Deer
Lk. M. Islands
Vhalley

Chapman
Chapman
Chapmadcroft
Spence
Spence
Spence
Monteith
Montieth
Ryerson
Machar
Machar
Machar
Lount
hunt
ChapHnan/Croft

cm*
McCoy
Hay
McKenzie
Lit. Boulter
Lk. St. Peter
Whitefish
Rock
Louisa
H w
Cache
Source
Potter
Brule

kck
Sabine
Sabine
SabineILyell
McClure
McClure
Sprsule
Nightingale
Lawrence
Lawrence
Canisbay
Peck
PwWHunter
Hunter
Hunter

C ~ P
Lucky
Ohlmmn
Reid
Big Bhlmann
Ban's
Fortune
tong Schooner
Kitchen
Mackie
Shaw
Bmle
endstone
Will's
Buckshot

Miller
Miller
Miller
Miller
Miller
Miller
Miller
Miller
Miller
Miller
Miller
Miller
Miller
CBarendon
Miller

.Toe

Cm. J. Fish. Aquat. Sci., 1101- 459 I988

(pg eQ/g d v mass)

TABLE1. (Csnckerded)
Cd in Pi. azteca
Lake
Echo
Ril
Chub
Little Wren
Beech
Maple
Green
Pine
Cranberry

Hv

Lake of Bays
Heeney
Dickie
Plastic
Blue Chalk
Red Chalk

( ~ Cd/g
g dry mass)

Township
Mckan
Ridout
Ridout
Sherbome
Stanhope
Stmhope
Guilfo1.8
Guilford
Guilfsrd
Cbffey
Franklin
Mckm
McLaan
S herbome
Ridout
Ridout

The adequacy of the interpretations of the principal compnents was tested by multiple linear regression using the v k ables loading on the principal components as independent vmiables against Cd concentrations in H. cmztecce. Four sets of
independent variables were tested (Ca2 ,Cd, DOC; ANC, Cd,
DOC; pH, Cd, DOC; Mg2+,Cd, DOC). The model including
Ca2-, Cd, and DOC has the best fit as measured by the a-square,
and the regression is summapized in 'Table 5.
+

Cadmium concentrations in freshwater crustaceans are typically less than 1.0 pg/g dry mass (Zauke I982b; Jop and
Wojtan 1982; Pfosi 1983). Concentrations in excess of 2 pg/g
are generally associated with industrial contamination (Anderson et al. 1978; Kneip and Hazen 1979; Zauke 1981; Jop and
Wo~tan1982;Ddlinger and Kautzky 1985j. Excluding the value
of 56.5 pg/g dry mass obtained for a single specimen from
Plastic Lake, Cd concentrations in H . ceztecce from central
Ontario lakes ranged from 0.13 to 3'9.3 pg/g dry mass. Both
the highest (Heeney Lake) and the lowest (Ohlmmn Lake) concentrations were recorded in remote lakes without known direct
sources of contamination.
Multiple linear regression of Cd concentrations in H . azteca
with the orthogonal-derived vaiiables (principal components)
showed that at least Qkree components account for significant
amounts of variation. Two principd components (PC%,PC3)
have unambiguous interpretations (DOC and total Cd concentrations, respectively). However, PC 1 was strongly correlated
with Ca2 , Mg2+,pH, and ANC. Its interpretation is ambiguous and must focus on whether hardness cations or ANC
(HC0,-, C0,2-) modify the availability of Cd to H . aztecce.
Interactions between water hardness and trace metal toxicity
are well documented. It is thought that the protection afforded
by hardness is due to competition between divalent base (Ca2+,
Mg2+)and trace metal cations for binding sites, thereby reducing uptake and toxicity, Cadmium toxicity to G w m m s pulex
is reduced by high Ca concentrations (Wright and hain 198I),
and the process of Cd accumulation has been linked with Ca
metabolism (Wright 198Q).At "low" Cd concentrations (56 560 pg/L), arn equimolmrelationship between @aand Cd uptake
was implied by Wright (1980). This conclusion is partly SUPported by data from the present study. Although Cd concentra+

TABLE2. Variables included in the full K A matrix, their geometric means, and ranges.

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Variable

Mean

Rmge

ANC (mqlL)
Total P (pglL)
Ca b @ L )
Mg (mgW
Na (mg/L)
K (mg/L)
F oJ&L)
C1 (mg/L)
so4 (mdL)
Total Fe (m@L)
Total Mn (mg/L)
DOC (mg/L)

PH

Total Cd in sediment (mg/kg dry mass)

Sediment loss on ignition (5%)
Total @d in water (ng/L)
Maximum depth (m)
Mean depth (m)
Lake area (ha)
M e perimeter (b)
TABLE3. Loadings of enviromental variables on principal compsRents, and percentage of the overall variance accounted for by each
component, Loadings of absolute value greater than 0.50 are
underlined.
Variable
Ca
PH
ANC
Mi3
DOC
Total Cd
% of total variance

PC 1

PC2

PC3

0.965
0.902
0.882
0.874
- 0.087
-0.312

0.054
-0.048
0.220
8.122
-0.994
0.055

- 0.179
- 0.352
- 0.360

56.51

-0.114
- 0.043
0.948

17.65

19.98

TABLE4. Stepwise multiple linear regression of log-transformed Cd

concentrations in H.arteco versus principal components for 5 1 lakes
- -

Variable

TABLE5. Stepwise multiple linear regression of log-transformed @d

concentrations in H. azteca versus Ca, Cd, md DOC in water for
5 1 lakes in central Ontario.
Variable

SE

0.264
0.148
0.101
0.241

4.47
-7.78
6.36
-3.35

C0.001
<0.001
<8.001
-0.002

Coefficient

Intercept
Ca
@d
DOC

1.182
- 1.154

0.643

- 0.805

r = 0.901
r2 = 0.813
-

- -

Analysis of variance
Source
Regression

df

Sum square

Mean square

15.801
3.645

5.267
0-078

67.92

<0.001

47

Coefficient

Intercept
PC1
K 2
PC3

0.580
- 0.424

0.132
0.342

BP

SE

0.039
0.040
0.040
0.040

14.70

<0.001
<0.001
0.002
C8.001

- 10.64

3.31
8.60

r = 8.898
r2 = 0.808

Analysis of variance
Source

df

Sum square

Mean square

Regression
Residual

3
47

15.717
3,728

5.239
0.079

66.04

<0.001

tions in H. azteca fmm lakes in the Sudbury area are high,

reflecting the elevated Cd concentrations in lake water, they are
not elevated when expressed as a function of the Cd:Ca mots
ratio in lake water. The relationship between Cd concentrations
in H . azteca and the Cd:Ca molar ratio in I&e water (Fig. 2)
has a slope of 0.843 (SE = 0.072) which is significantly less
@ < 0.05) than 1. A slope of 1 would suggest that H. azteca
cannot discriminate between Cd and Ca cations during uptake

and excretion. The lower value indicates that some discrimination, either during uptake (i.e. by the cation pump at the gill
surface) or via depuration (selective Cd Boss during excretion,
d y s i s , or other mechmism), may occur.
The second interpretation of PCB (a gradient of increasing
pH and AN@)is the expectation of an interaction between Cd
and bicxbonslbe/cxbonate species which could effectively
complex Cd a d reduce the available cationic fraction of the
total Cd concentration. Gardiner (1974) explored Cd speciation
with a variety of inorganic and organic ligands, using a Cdspecific electrode. He concluded that there was strong evidence
for a soluble Cd.+x.rbonate complex. However, this complex is
weak and only %omsat pH > 8.0. Under conditions typical of
central Ontario lakes, it is unlikely that Cd4xbonate complex
fornation could significantly modify the Cd bioavailability.
High concentrations of DOC reduce Cd concentrations in
H. azteca. The effect of DOC on trace metal bbiavailability is
due to the cheldion or complexation of trace metal ions, largely
onto hnrmic and fnrlvic acids (Neubecker and Allen 1983). Eaboratory studies (Poldoski 1979; Geisy et id. 1977; Dressing et
al. 1982; Winner 1984; Oakden et al. 1984) show that various
size fractions of natural dissolved organic matter, or synthetic
Can. J. Fish. Aquat. Sei., Val. 45, I988

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Cd:Ca MOLAR RATIO IN LAKE WATE R

FIG. 2. Cd concentrations in H.aateca versus Cd:Ca molar ratios in 1&e water. The fitted line is
described by the equation Iog ( ~ C&g
g dry mass) = 0.832 (Bog Cd:Ca molar ratio) + 0.602 (n = 51,
r = 0.86, p < 0.081).

chelators, may increase or decrease the bioavailability or toxicity of Cd to invertebrates. The net effect of high DOC concentrations in central Ontario lakes is to decrease the availability of Cd to H . azteca, although PC2 (interpreted as DOC)
is much less important as a predictor of Cd concentrations in
H.azteca than PC1 (Ca2+,h4g2+,ANC, pH) and PC3 (total
Cd).

Conclusion
Cadmium concentrations in 8%. azteca are correlated with
water chemistry md are independent of sediment Cd concentrations and basin monphometry. Thee chemical parameters
(Ca2+,total Cd, DOC) explain 8 B -3% of the total variation in
Cd concentrations of H. azteca. It is likely that Ca2+and Cd
compete for uptake, while DOC may complex a portion of the
total aqueous Cd, reducing the available ionic Cd concentration.

BORG,H. 1983. Trace metals in Swedish natural fresh waters. Hydrobiologia

101: 27-34.

CHAN,W. H., A. J. S- TANG,D. H. S. C ~ U P I G

AND
, M. A. LUSIS. 1986.
Concentration and deposition of trace metals in Ontario - 1982. Water
Air Soil Pollut. 29: 373-389.
DALLINGER,
R., AND H.KAUTZKY.
1985. The passage of Cu, Zn, Cd and Pb
along a short food chain into the fish Salmo gairdneri, p. 694-4596. In
T. D.k U a s led.] PPoceedings of the International Conference on Heavy
Metals in the Environment. Vol. 1. Athens. CEP Consultants, Led.,
Edinburgh.
DAVID,K. A. 1952. Upper 5 and 1% points of the maximum 6;-ratio. Bismetrika 39: 422424.
DRESS~G,
S. A., R. P. MAAS,AND C. M. WEISS. 1982. Effect of chemical
speciation on the accumulation of cdmium by the caddisfly, Hydropsyche
sp. Bull. Environ. Contm. Toxicol. 28: 172-180.
GARDINER,
J. 1974. The chemistry of cadmium in natural water - I. A study
of cadmium complex formation using the cadmium-specific ion electrode,
Water Res . 8: 23-30.
GEISY,B. P., G. %.LEVERSEE,
AND D. R. WILLIAMS.1977. Effects of naturally
occurring aquatic sganic fractions on cadmium toxicity to SimocephPsts
sergeflatus(Daphnidae) and Cambusia afznis (Pwiliidae). Water Res. 11:
1013-1020.

This paper formed a part sf the Doctoral thesis of M. Stephenson.

The input and critical comments of my Supervisor and Committee
(DKs.G . E. Mackie, P. J. Billon, T. B. Nudds, L C. Woff), N. B.
Ym, md D. W. Schhdler are gratefully acknowledged. 8. Twlarnd
assisted with field smpIhg. P. J. Billon (Ontario Ministry of the Environment) provided water chemistry analysis. 6.Gale (Ontario Ministry of Natural Resources) provided lake mnsrphometric data. D.
Strickland (OMNIP) granted permission to sample lakes in Algonquin
Park. Funding was provided by NSEWC grant No. GO918, m quipment grant from Xerox Cmada, md by Xerox and Ontario Graduate
Scholarships.

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